Sea louse infection of juvenile sockeye salmon in relation to marine salmon farms on Canada's west coast

Background

Pathogens are growing threats to wildlife. The rapid growth of marine salmon farms over the past two decades has increased host abundance for pathogenic sea lice in coastal waters, and wild juvenile salmon swimming past farms are frequently infected with lice. Here we report the first investigation of the potential role of salmon farms in transmitting sea lice to juvenile sockeye salmon (Oncorhynchus nerka).

Methodology/Principal Findings

We used genetic analyses to determine the origin of sockeye from Canada''s two most important salmon rivers, the Fraser and Skeena; Fraser sockeye migrate through a region with salmon farms, and Skeena sockeye do not. We compared lice levels between Fraser and Skeena juvenile sockeye, and within the salmon farm region we compared lice levels on wild fish either before or after migration past farms. We matched the latter data on wild juveniles with sea lice data concurrently gathered on farms. Fraser River sockeye migrating through a region with salmon farms hosted an order of magnitude more sea lice than Skeena River populations, where there are no farms. Lice abundances on juvenile sockeye in the salmon farm region were substantially higher downstream of farms than upstream of farms for the two common species of lice: Caligus clemensi and Lepeophtheirus salmonis, and changes in their proportions between two years matched changes on the fish farms. Mixed-effects models show that position relative to salmon farms best explained C. clemensi abundance on sockeye, while migration year combined with position relative to salmon farms and temperature was one of two top models to explain L. salmonis abundance.

Conclusions/Significance

This is the first study to demonstrate a potential role of salmon farms in sea lice transmission to juvenile sockeye salmon during their critical early marine migration. Moreover, it demonstrates a major migration corridor past farms for sockeye that originated in the Fraser River, a complex of populations that are the subject of conservation concern.     

Tendencies of Density Dynamics in Reophilic and Lacustrine Sockeye Salmon Oncorhynchus nerkain the Basin of Azabach'e Lake

Temporal series of density in the spawners of two sockeye salmon populations from Azabach'e Lake (Kamchatka River basin) were analyzed using periodic functions. It has been found that the quality of describing the density dynamics for sockeye salmon by such models is very high (R ²= 0.943 and R ²= 0.905 for early and late populations, respectively). The density (for early sockeye salmon) and total number (for late sockeye salmon) distributions of the reproductive fraction of the populations have been developed and analyzed.     

MOLECULAR GENETIC EVIDENCE FOR PARALLEL LIFE-HISTORY EVOLUTION WITHIN A PACIFIC SALMON (SOCKEYE SALMON AND KOKANEE,ONCORHYNCHUS NERKA)

The Pacific salmon Oncorhynchus nerka typically occurs as a sea-run form (sockeye salmon) or may reside permanently in lakes (kokanee) thoughout its native North Pacific. We tested whether such geographically extensive ecotypic variation resulted from parallel evolutionary divergence thoughout the North Pacific or whether the two forms are monophyletic groups by examining allelic variation between sockeye salmon and kokanee at two minisatellite DNA repeat loci and in mitochondrial DNA (mtDNA) Bgl II restriction sites. Our examination of over 750 fish from 24 populations, ranging from Kamchatka to the Columbia River, identified two major genetic groups of North Pacific O. nerka: a “northwestern” group consisting of fish from Kamchatka, western Alaska, and northwestern British Columbia, and a “southern” group consisting of sockeye salmon and kokanee populations from the Fraser and Columbia River systems. Maximum-likelihood analysis accompanied by bootstrapping provided strong support for these two genetic groups of O. nerka; the populations did not cluster by migratory form, but genetic affinities were organized more strongly by geographic proximity. The two major genetic groups resolved in our study probably stem from historical isolation and dispersal of O. nerka from two major Wisconsinan glacial refugia in the North Pacific. There were significant minisatellite DNA allele frequency differences between sockeye salmon and kokanee populations from different parts of the same watershed, between populations spawning in different tributaries of the same lake, and also between sympatric populations spawning in the same stream at the same time. MtDNA Bgl II restriction site variation was significant between sockeye salmon and kokanee spawning in different parts of the same major watershed but not between forms spawning in closer degrees of reproductive sympatry. Patterns of genetic affinity and allele sharing suggested that kokanee have arisen from sea-run sockeye salmon several times independently in the North Pacific. We conclude that sockeye salmon and kokanee are para- and polyphyletic, respectively, and that the present geographic distribution of the ecotypes results from parallel evolutionary origins of kokanee from sockeye (divergences between them) thoughout the North Pacific.     

Olfactory gene expression in migrating adult sockeye salmon Oncorhynchus nerka

Expression of 12 olfactory genes was analysed in adult sockeye salmon Oncorhynchus nerka nearing spawning grounds and O. nerka that had strayed from their natal migration route. Variation was found in six of these genes, all of which were olfc olfactory receptors and had lower expression levels in salmon nearing spawning grounds. The results may reflect decreased sensitivity to natal water olfactory cues as these fish are no longer seeking the correct migratory route. The expression of olfactory genes during the olfactory‐mediated spawning migration of Pacific salmon Oncorhynchus spp. is largely unexplored and these findings demonstrate a link between migratory behaviours and olfactory plasticity that provides a basis for future molecular research on salmon homing.     

Impact of parasites on salmon recruitment in the Northeast Atlantic Ocean

Parasites may have large effects on host population dynamics, marine fisheries and conservation, but a clear elucidation of their impact is limited by a lack of ecosystem-scale experimental data. We conducted a meta-analysis of replicated manipulative field experiments concerning the influence of parasitism by crustaceans on the marine survival of Atlantic salmon (Salmo salar L.). The data include 24 trials in which tagged smolts (totalling 283 347 fish; 1996–2008) were released as paired control and parasiticide-treated groups into 10 areas of Ireland and Norway. All experimental fish were infection-free when released into freshwater, and a proportion of each group was recovered as adult recruits returning to coastal waters 1 or more years later. Treatment had a significant positive effect on survival to recruitment, with an overall effect size (odds ratio) of 1.29 that corresponds to an estimated loss of 39 per cent (95% CI: 18–55%) of adult salmon recruitment. The parasitic crustaceans were probably acquired during early marine migration in areas that host large aquaculture populations of domesticated salmon, which elevate local abundances of ectoparasitic copepods—particularly Lepeophtheirus salmonis. These results provide experimental evidence from a large marine ecosystem that parasites can have large impacts on fish recruitment, fisheries and conservation.     

The effect of the infectious hematopoietic necrosis virus on the population of sockeye salmon <Emphasis Type="Italic">Oncorhynchus nerka</Emphasis> (Salmoniformes,Salmonidae) from Lake Nachikinskoe

The results of virological examination of adult sockeye salmon Oncorhynchus nerka in Lake Nachikinskoe from 2003 to 2008 demonstrated high values of prevalence of the infectious hematopoietic necrosis virus (IHNV) in the fish population (up to 100%). In the studied water reservoir there are optimal conditions for the development and revealing of the epizootic of infectious hematopoietic necrosis (IHN). In Lake Nachikinskoe, two natural epizootics of IHN in juvenile sockeye salmon were recorded in 2003 and 2006. The tendencies for change of prevalence of IHNV by years were analyzed, and their relation to the numbers of adult sockeye salmon at the spawning grounds of Lake Nachikinskoe was determined. The correlation of IHNV prevalence with the numbers of adult sockeye salmon in the studied water reservoir is direct but insignificant (r _s = 0.695, p < 0.05). It was shown that the epizootic of 2003 could affect the fact that fish return in 2007 and 2008 was minimum for the considered time interval while the numbers of their parents were, on the other hand, very high.     

Algal picoplankton production and contribution to food-webs in oligotrophic British Columbia lakes

The pelagic communities of two contrasting oligotrophic lakes in British Columbia were studied to determine why an interior, dimictic lake (Quesnel) supports a greater biomass of zooplankton and produces larger planktivorous sockeye salmon (Oncorhynchus nerka) than a coastal warm-monomictic lake (Sproat). The ultra-oligotrophic status and differing planktivore densities in Sproat Lake increased the relative importance of algal picoplankton, diminished the abundance of large zooplankton, and increased the significance of rotifers and other small-bodied zooplankton. These picoplankton based food webs result in longer, indirect and less efficient pathways of carbon flow from phytoplankton to fish. In contrast, Quesnel Lake is a more productive oligotrophic lake and its pelagic food webs are based more on nanoplankton and small microphytoplankton that support larger-bodied zooplankton (Daphnia, Diaptomus), and a more direct and efficient two-step transfer to fish. The greater variability of the annual recruitment of sockeye fry in interior lakes may keep zooplankton communities in a non-steady state, this in turn may perpetuate the occurrence of quadrennial cyclic dominance in adult salmon returning to these systems.     

Parasitic castration of a vertebrate: Effect of the cymothoid isopod, Anilocra apogonae, on the five-lined cardinalfish, Cheilodipterus quinquelineatus

Parasitic castration, the specific blocking of host reproductive output by an individual parasite, is a host-parasite interaction common to many invertebrates, particularly crustaceans, echinoderms and molluscs. It can reduce host density, alter host population dynamics and the evolution of host life history traits. Here we show that parasitisation by a single female cymothoid isopod, Anilocra apogonae, castrates its vertebrate host, the five-lined cardinalfish, Cheilodipterus quinquelineatus. Parasitised male fish fail to mouthbrood their young. The gonads of parasitised fish are smaller and parasitised female fish have substantially fewer and smaller ova than do the gonads of unparasitised fish. As for parasitic castrators of invertebrate hosts, A. apogonae on C. quinquelineatus are uniformly dispersed amongst infested hosts (one adult female isopod per host), are site specific, and their body size is highly correlated with that of their host. These isopods are large relative to the body size of their hosts, averaging 3.8% of the weight of the host. Parasitised fish also weigh less and are shorter than unparasitised fish of the same age. Despite the presence of other potential hosts, A. apogonae only infests C. quinquelineatus. The consistency of the ecological correlates amongst known parasitic castrators suggests that the parasitic castrator host-parasite relationship will be recognised for other parasites of vertebrates.     

Reduced growth in wild juvenile sockeye salmon Oncorhynchus nerka infected with sea lice

Daily growth rings were examined in the otoliths of wild juvenile sockeye salmon Oncorhynchus nerka to determine whether infection by ectoparasitic sea lice Caligus clemensi and Lepeophtheirus salmonis was associated with reduced host body growth, an important determinant of survival. Over 98% of the sea lice proved to be C. clemensi and the fish that were highly infected grew more slowly than uninfected individuals. Larger fish also grew faster than smaller fish. Finally, there was evidence of an interaction between body size and infection status, indicating the potential for parasite‐mediated growth divergence.     

Juvenile sockeye salmon distribution, size, condition and diet during years with warm and cool spring sea temperatures along the eastern Bering Sea shelf

Interannual variations in distribution, size, indices of feeding and condition of juvenile Bristol Bay sockeye salmon Oncorhynchus nerka collected in August to September (2000–2003) during Bering–Aleutian Salmon International Surveys were examined to test possible mechanisms influencing their early marine growth and survival. Juvenile sockeye salmon were mainly distributed within the southern region of the eastern Bering Sea, south of 57°0' N during 2000 and 2001 and farther offshore, south of 58°0' N during 2002 and 2003. In general, juvenile sockeye salmon were significantly larger ( P < 0·05) and had significantly higher indices of condition ( P < 0·05) during 2002 and 2003 than during 2000 and 2001. The feeding index was generally higher for age 1.0 year sockeye salmon than age 2.0 year during all years. Among-year comparisons suggested that Pacific sand lance Ammodytes hexapterus were important components of the juvenile sockeye salmon diet during 2000 and 2001 (20 to 50% of the mean wet mass) and age 0 year walleye pollock Theragra chalcogramma were important components during 2002 and 2003 (50 to 60% of the mean wet mass). Warmer sea temperatures during spring and summer of 2002 and 2003 probably increased productivity on the eastern Bering Sea shelf, enhancing juvenile sockeye salmon growth.     

Geographical and host distribution patterns of Parvicapsula minibicornis (Myxozoa) small subunit ribosomal RNA genetic types

Parvicapsula minibicornis is a myxozoan parasite implicated in mortalities of both juvenile and pre-spawning adult salmon in the Pacific Northwest of North America. Disease severity and presentation varies between salmon species and geographical localities. To better characterize population structure of the parasite, we sought genetic markers in the P. minibicornis ribosomal RNA gene. We compared samples from California with the type specimen from British Columbia, identified sequence variations, and then sequenced 197 samples from fish, river water and the parasite's polychaete worm host. Although DNA sequences of the parasite were >98·9% similar, there was enough variation to define 15 genotypes. All genotypes were detected in fish samples, although not in all species. A single genotype only was found in sockeye and pink salmon in the Fraser River Basin, but was not detected in sockeye from the adjacent Columbia River Basin. All coho salmon, irrespective of river basin, were infected with a unique mix of 2 genotypes. These data indicated that the P. minibicornis population exhibited strong signals of structuring by both geography and salmonid host species. Particular genotypes may correlate with disease differences seen in salmon populations in the Pacific Northwest.     

Regulation of wing formation and adult development in an aphid host, Aphis fabae, by the parasitoid Aphidius colemani

Nymphs of presumptive winged gynoparae of Aphis fabae (Hemiptera: Aphididae), were exposed to female parasitoids, Aphidius colemani (Hymenoptera: Aphidiidae) and stung once with the ovipositor. Wing development was inhibited and, when aphids were parasitised during the early stages, they did not reach the adult stage but mummies with rudimentary or no wingbuds are observed in the host's fourth-stadium. These and previous studies have suggested that wing development may be inhibited by factor(s) from the maternal parasitoid injected into the host at the time of oviposition. In an attempt to identify such factor(s), saline extracts of whole female parasitoids, abdomens, ovaries and venom glands were prepared. When a saline extract of venom glands was injected into late-second-stadium aphids, many develop to fourth-stadium nymphs with rudimentary wingbuds, indicating an effect on wing formation but also showed developmental arrest and often died when attempting to moult to the adult stage. It appears that host death may be related to physiological/biochemical interactions of parasitoid and host rather than just late stage parasitoid larvae ingesting the host's vital organs. Injections with extracts into later host stadia gave similar results with regard to development to the adult, although aphids injected in the late-fourth-stadium develop normally to the adult stage with no effect on wing formation. The results indicate that the earlier the injection before the final moult the greater the effect of the injected extract on preventing adult development.Extracts prepared from head + thorax do not affect aphid development and the results indicate that there is an active factor(s) - likely a protein - in the female parasitoid's venom that disrupts wing development and/or inhibits development to the adult stage. Surprisingly, injections of extracts from male parasitoids have similar effects but the location and function of such a factor(s) in males are unknown.     

A wide window of migration phenology captures inter‐annual variability of favourable conditions: Results of a whole‐lake experiment with juvenile Pacific salmon

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Differences in host selection of actinospores of two myxosporeans, Myxobolus arcticus and Thelohanellus hovorkai

We investigated the host selection mechanism of actinospore stages of 2 myxosporeans, Myxobolus arcticus and Thelohanellus hovorkai, infecting masu salmon (Oncorhynchus masou) and common carp (Cyprinus carpio), respectively. Discharge of the polar filaments and sporoplasm release by M. arcticus actinospores occurred within the first 5 min of exposure to skin mucus of masu salmon. The actinospores also reacted to the mucus of nonsusceptible fish, i.e., sockeye salmon (Oncorhynchus nerka) and goldfish (Carassius auratus), although the reactivity was comparatively lower. After exposure of masu, and sockeye and chum salmon (Oncorhynchus keta) to M. arcticus actinospores, the penetration of sporoplasms was observed in the fins and gills of masu and sockeye salmon to a similar extent and to a lesser extent in chum salmon. Thelohanellus hovorkai actinospores exhibited a slow response of sporoplasm release to common carp mucus as well as penetration into the gills of common carp. Neither chemoresponse to mucus of nonsusceptible fish (goldfish and sockeye salmon) nor sporoplasm invasion in goldfish was observed for T. hovorkai actinospores. These results indicate notable differences in the host selection at the time of entry between M. arcticus and T. hovorkai; the former responds quickly to fish mucus with low host specificity, whereas the latter was highly host specific in a dilatory reaction.     

The effect of Achyranthes japonica extract on larval survival and development and oviposition behavior of Plutella xylostella L. (Lepidoptera: Plutellidae)

The extract of Achyranthes japonica was tested for effects on larval survival and development and the oviposition behavior of the diamondback moth, Plutella xylostella L. Chinese cabbage dipped in A. japonica extract solution showed 51–80% antifeedant activity for 5 days against P. xylostella larvae, and more larvae were also on untreated cabbage leaves 24 h after release. The mortality of P. xylostella larvae increased proportionally to the duration of dipping time in the extract, and both pupation and emergence rates of larvae feeding only on treated cabbage were lower than those for larvae raised on untreated or with a choice of cabbage. The 20-hydroxyecdysone (20E) concentration in leaves was approximately 549, 1232, 1275, and 1426 μg/g at 6, 12, 24, and 48 h after dipping treatment, respectively. Notably, naive females laid more eggs on untreated cabbage than on treated cabbage, and females from larvae raised on treated Chinese cabbage also preferred the non-treated leaves. Our results are in contrast to those from earlier studies using various insect models that confirmed most females prefer to lay eggs on the host type that was eaten in the larval stage (Hopkins host selection principle). Cabbage dipped in the A. japonica solution for 24 h caused 59% larval mortality and inhibited both pupation and emergence rates of the larvae when exposed to plants 15 and 22 days after planting in the field, with the 20E concentration in the treated cabbage leaves at 1600.9 ± 122.36 and 1386.8 ± 24.69 μg/g, respectively. Therefore, the biological effectiveness could be attributed to the 20E in the treated cabbage leaves.     

Expression of a Novel Piscine Growth Hormone Gene Results in Growth Enhancement in Transgenic Tilapia (Oreochromis Niloticus)

Several lines of transgenic G1 and G2 tilapia fish (Oreochromis niloticus) have been produced following egg injection with gene constructs carrying growth hormone coding sequences of fish origin. Using a construct in which an ocean pout antifreeze promoter drives a chinook salmon growth hormone gene, dramatic growth enhancement has been demonstrated, in which the mean weight of the 7 month old G2 transgenic fish is more than three fold that of their non transgenic siblings. Somewhat surprisingly G1 fish transgenic for a construct consisting of a sockeye salmon metallothionein promoter spliced to a sockeye salmon growth hormone gene exhibited no growth enhancement, although salmon transgenic for this construct do show greatly enhanced growth. The growth enhanced transgenic lines were also strongly positive in a radio-immuno assay for the specific hormone in their serum, whereas the non growth enhanced lines were negative. Attempts to induce expression from the metallo thionein promoter by exposing fish to increased levels of zinc were also unsuccessful.Homozygous transgenic fish have been produced from the ocean pout antifreeze/chinook salmon GH construct and preliminary trials suggest that their growth performance is similar to that of the hemizygous transgenics. No abnormalities were apparent in the growth enhanced fish, although minor changes to skull shape and reduced fertility were noted in some fish. There is also preliminary evidence for improved food conversion ratios when growth enhanced transgenic tilapia are compared to their non-transgenic siblings.The long term objective of this study is to produce lines of tilapia which are both growth enhanced and sterile, so offering improved strains of this important food fish for aquaculture.     

Clove oil as an anaesthetic for adult sockeye salmon: field trials

Wild migrating sockeye salmon Oncorhynchus nerka exposed to 20, 50 and 80 mg 1⁻¹ of clove oil could be handled within 3 min, recovered within 10 min, and survived 15 min exposure trials. Fish tested at 110 mg 1⁻¹ did not recover from 15 min exposure trials. Response curves developed for induction and recovery time considered the following predictors: clove oil concentration, sex, fish length and depth. A significant positive dependence was observed between induction time and fish length for 20, 50 and 80 mg 1⁻¹ test concentrations; no dependence was observed between induction time and length at 110 and 140 mg 1⁻¹. Recovery time differed as a function of clove oil concentration, but not fish size. A concentration of 50 mg 1⁻¹ is recommended for anaesthetizing sockeye salmon ranging in length from 400 to 550 mm at water temperatures averaging 9–10° C.     

Prey selection and efficiency of naïve and experienced juvenile sockeye salmon

Prey selection and growth efficiency of juvenile sockeye salmon Oncorhynchus nerka switched between live prey and pelleted diets were investigated. First feeding sockeye salmon fry were placed into one of three dietary treatments for 7 months prior to assessing potential differences with a growth and a behavioural assay. Dietary treatments were (1) adult Artemia franciscana for 1 month, followed by pelleted feed for an additional 6 months ( Art − BD), (2) pelleted feed from first feeding for 7 months (BD) and (3) adult A. franciscana for 1 month, and a combination of pelleted feed and live adult A. franciscana for 6 months ( Art + BD). Equal numbers from each treatment group were then tagged, pooled into replicate 'common garden' tanks and fed novel live prey items ( Daphnia sp. and mosquito Culex pipiens larvae) for an additional 3 weeks. No significant differences in the growth efficiency of sockeye salmon were found during the 3 week feeding trial on the novel prey items. Additional sockeye salmon from each dietary treatment were used in a behavioural assay to determine if the treatments had an impact on foraging efficiency (prey selection or time to capture prey). No significant differences in prey selection were found among treatment groups in time to capture pellets, A. franciscana or mosquito larvae. Also, no significant differences were found within treatment groups in time to capture different food sources. No substantive benefits in foraging efficiency of sockeye salmon associated with prior exposure to live prey were demonstrated. This suggests that altering existing hatchery practices for juvenile sockeye salmon by offering live food prior to release is unlikely to influence post-hatchery feeding behaviour or increase post-release survival.     

Lacustrine growth of juvenile pink salmon and a comparison with sympatric sockeye salmon

The growth rates of naturally sympatric juvenile pink Oncorhynchus gorbuscha and sockeye Oncorhynchus nerka salmon were compared in a common lacustrine environment in south‐west Alsaka, an unusual opportunity given the normal disparity in freshwater residence time of these two species. Fork length ( L _F) frequency distributions of juvenile pink salmon caught in the lake during the summer in 1991 and 1999–2003 indicated a growth rate of 0·54 mm day⁻¹, 54% greater than the estimated growth rate of juvenile sockeye salmon sampled from 1958 to 2003 (0·35 mm day⁻¹). Examination of daily growth rings on otoliths indicated that pink salmon in Lake Aleknagik grew an average of 1·34 mm day⁻¹ in 2003 but sockeye salmon grew only 0·63 mm day⁻¹(average specific growth rates were 3·0 and 1·8% day⁻¹, respectively). Pink salmon increased from c . 32 mm L _F and 0·2 g at emergence to 78 mm L _F and 3·0 g within 3–4 weeks. After experiencing these rapid growth rates, the pink salmon appeared to leave the lake by late July in most years. The diets of pink and sockeye salmon in the littoral zone of the lake were very similar; >80% of the stomach contents consisted of adult and pupal insects and the remainder was zooplankton. This high degree of diet overlap suggested that the observed differences in growth rate were not attributable to variation in prey composition.